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Circadian Rhythms in Adipose Tissue Physiology

Jana‐Thabea Kiehn, Anthony H. Tsang, Isabel Heyde, Brinja Leinweber, Isa Kolbe, Alexei Leliavski, Henrik Oster

10.1002/cphy.c160017

Source: Volume 7, Issue 2, April 2017

Published online: March 2017

Full Article on Wiley Online Library



ABSTRACT

The different types of adipose tissues fulfill a wide range of biological functions—from energy storage to hormone secretion and thermogenesis—many of which show pronounced variations over the course of the day. Such 24‐h rhythms in physiology and behavior are coordinated by endogenous circadian clocks found in all tissues and cells, including adipocytes. At the molecular level, these clocks are based on interlocked transcriptional‐translational feedback loops comprised of a set of clock genes/proteins. Tissue‐specific clock‐controlled transcriptional programs translate time‐of‐day information into physiologically relevant signals. In adipose tissues, clock gene control has been documented for adipocyte proliferation and differentiation, lipid metabolism as well as endocrine function and other adipose oscillations are under control of systemic signals tied to endocrine, neuronal, or behavioral rhythms. Circadian rhythm disruption, for example, by night shift work or through genetic alterations, is associated with changes in adipocyte metabolism and hormone secretion. At the same time, adipose metabolic state feeds back to central and peripheral clocks, adjusting behavioral and physiological rhythms. In this overview article, we summarize our current knowledge about the crosstalk between circadian clocks and energy metabolism with a focus on adipose physiology. © 2017 American Physiological Society. Compr Physiol 7:383‐427, 2017.

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Figure 1. Figure 1. Molecular dynamics of the mammalian clock's core TTL. BMAL1:CLOCK (B and C, respectively) heterodimers bind to E‐Box motifs in the promotor regions of target genes and promote transcription of Period (Per, P) and Cryptochrome (Cry, C) genes in the morning. Over the following hour, PER and CRY proteins accumulate in the cytoplasm and are rapidly degraded following phosphorylation by CK1s and AMPK/GSK3ß, respectively. At the beginning of the dark phase, PER and CRY complexes form, stabilizing both proteins against degradation and initiating translocation into the nucleus. Nuclear PER:CRY complexes inhibit the transactivational activity of BMAL1:CLOCK during the night, thus blocking Per/Cry transcription. Toward the morning, PER and CRY levels in the nucleus decline, releasing BMAL1:CLOCK repression, and initiating a new circadian cycle.
Figure 2. Figure 2. Interlocking TTLs within the mammalian circadian clockwork. The positive limb of the pace making core TTL comprises of the two transcription factors BMAL1 and CLOCK, whereas the PERs and CRYs form its negative limb. Several auxiliary TTLs reinforce stabilization and robustness of the 24‐h oscillation. Rev‐ERBs and RORs repress or stimulate the transcription of Bmal1, respectively. In addition, E4bp4 transcription is regulated by REV‐ERBs/RORs and E4BP4 protein represses Per2 expression. Dbp transcription is activated by BMAL1:CLOCK and DBP activates Per1 transcription via D‐box binding. Transcription of the two Dec genes is regulated by BMAL1:CLOCK and DEC proteins represses CLOCK:BMAL1 transactivation, similar to PER:CRY complexes.
Figure 3. Figure 3. Hierarchical organization of the mammalian circadian clock system. The different clocks within the mammalian organism are organized in a hierarchical manner. A master clock in the SCN receives light information via retinal ipRGC and integrates this information to coordinate circadian rhythms of non‐SCN CNS and peripheral oscillators. The SCN resets peripheral oscillators via regulation of hormonal rhythms (e.g., melatonin), through rhythmic autonomic innervation, or indirectly through the regulation of body temperature and behavioral functions such as sleep/wake and food intake cycles.
Figure 4. Figure 4. Zeitgebers entrain endogenous rhythms to the 24‐h day cycle. (A) The SCN clock controls rest/activity rhythms in rodents. In constant environmental conditions (constant darkness, DD) mice show locomotor free‐running rhythms with periods below 24 h (left). Under 12‐h light: 12‐h dark (LD) cycle locomotor rhythms are entrained to the external 24‐h period (right). (B) Peripheral clock function can be monitored by measuring luminescence from a clock promoter‐driven luciferase construct such as Bmal1:Luc in cultivated cells or tissues. After synchronization tissue clocks free‐run with an endogenous period of close to, but not exactly, 24 h (left). By applying rhythmic temperature cycles these rhythms become entrained to a 24‐h period (right). In a similar way peripheral tissues are entrained by the SCN pacemaker in vivo.
Figure 5. Figure 5. Central and peripheral circadian clocks are synchronized to the 24‐h day by different zeitgebers. Light is the most potent zeitgeber in mammals. Photic information is transmitted to the SCN via ipRGCs. In poikilothermic organisms, temperature fluctuations can also directly affect the circadian pacemaker. Tight coupling of neuronal firing within the SCN resets the SCN clock. From there, time information is passed on to peripheral oscillators. Experiments with transgenic mice have recently shown that SCN clock function is principally not necessary to transmit light information to peripheral clocks, but the mechanisms of this pathway remain largely unclear. In contrast to light, food intake can reset peripheral clocks independent of the SCN via peripheral hormonal and metabolite signals.
Figure 6. Figure 6. Adipose tissue depots. WAT (A, C) and BAT (B, D, E) are differently localized in rodents (A, B) and humans (C‐E). (A) In rodents, WAT is found at subcutaneous, visceral (surrounding the inner organs), and intramuscular sites. Visceral depots are further divided into cervical (in the neck), mesenteric (attached to the intestine), retroperitoneal, perirenal (around the kidney), gonadal, and inguinal (in the groin) pads. (B) BAT is mainly localized between the shoulder blades (interscapular). Smaller depots are found at cervical, axillary, mediastinic, and perirenal sites. (C) In humans, WAT is also principally divided into subcutaneous, visceral, and intramuscular depots. The most prominent subcutaneous WAT depots are localized abdominally and gluteofemorally (at the buttocks and thighs). Visceral depots are spread very broadly throughout the body and divided into pericardial (around the heart), omental (near to the stomach and spleen) peri‐ and pararenal, mesenteric, retroperitoneal, and gonadal pads. (D) In infants large BAT depots are located between the shoulder blades (interscapular), while (E) in adults more widespread, but less distinct depots are found at cervical, interscapular, para‐aortic, paravertebral, and suprarenal sites.
Figure 7. Figure 7. Modern lifestyle factors promote chronodisruption. Different lifestyle factors such as irregular and nighttime food intake, reduced activity, irregular and disrupted sleep and shift work as well as nocturnal exposure to artificial light perturb natural zeitgeber rhythms, disrupting phase coherence between different tissue clocks. Circadian clock misalignment promotes general chronodisruption, promoting the development of various diseases including metabolic dysfunction, cancer, and neuropsychiatric disorders.
Figure 8. Figure 8. Clock gene‐controlled regulation of adipose tissue differentiation. BMAL1:CLOCK regulates BAT adipogenesis through coordination of BMP and TGF‐ß signaling. It also inhibits WAT adipogenesis by activation of WNT pathways. REV‐ERBα induces WAT adipogenesis through stimulation of PPARγ and C/EBPα signaling.
Figure 9. Figure 9. Clock gene‐controlled regulation of WAT lipolysis. Local adipocyte clocks regulate TG breakdown and FFA release through CLOCK:BMAL1 controlled expression of rate limiting enzymes such as HSL, ATGL, and TGH.
Figure 10. Figure 10. Clock gene‐controlled regulation of BAT thermogenesis. BAT circadian oscillators regulate non‐shivering thermogenesis through REV‐ERBα‐mediated suppression of UCP1 expression. At the same time, the BAT clock machinery controls thermogenesis by limiting BAT differentiation through balancing TGF‐ß and BMP signaling in BAT preadipocytes. Of note, the expression of Rev‐erbα itself is downregulated by a thermogenesis inducing cold stimulus.
Figure 11. Figure 11. Adipose specific clock disruption in mice reveals a peripheral feedback mechanism controlling feeding behavior. The SCN synchronizes adipose clocks through endogenous zeitgebers including endocrine factors and behavioral rhythms such as feeding. Adipocyte‐derived and systemic factors together coordinate adipose physiology. Adipocyte‐specific KO of the essential clock gene Bmal1 reveals an adipose clock controlled regulation of polyunsaturated FFA release. Lack of polyunsaturated FFAs in adipose clock‐deficient mice leads to disinhibition of appetite, hyperphagy, and obesity.
Figure 12. Figure 12. The role of GC rhythms in the regulation of WAT physiology. The SCN controls circadian release of GCs from the adrenal via combined neuronal and endocrine pathways. Direct GABAergic projections from the SCN reach the PVN and the subparaventricular zone. From the PVN, CRH is released into the hypophyseal portal system to stimulate secretion of ACTH. ACTH, in turn, induces GC production and secretion in the adrenal cortex. In parallel, from PVN neurons sympathetic ganglia reach via the pituitary and the IML to innervate the adrenal medulla and, to a lesser extent, cortex, regulating sensitivity of the adrenal to ACTH stimulation. Upon binding to GR, GCs exert multiple effects on adipose tissue including the stimulation of lipolysis through activation of ATGL, HSL, and MGLL and of TG uptake through activation of LPL. GCs can also reset adipocyte clocks via induction of Per gene transcription. At the same time, local GC sensitivity is regulated by the adipocyte clock machinery, through CRYs and CLOCK:BMAL1 regulating GR availability and expression, respectively.
Figure 13. Figure 13. The role of melatonin rhythms in the regulation of BAT physiology. SCN regulates circadian rhythms of melatonin release from the pineal gland via a multisynaptic pathway involving the PVN and the IML of the spinal cord. Melatonin can feed back on SCN clock function through MT1/2 signaling. The main regulator of circadian rhythms of BAT activity is the SNS, through activation of ß3‐adrenergic receptor by NE. Melatonin modulates ß3‐AR signaling by inhibiting downstream adenylate cyclase activity and activating CREB through PKC‐mediated signals. At the same time melatonin signaling activates RORa expression through Gaq signaling, which, in turn, counteracts REV‐ERBα‐mediated suppression of UCP1.
Figure 14. Figure 14. The role of insulin in the regulation of WAT physiology. Baseline circadian blood levels of insulin are regulated by the SCN through sympathetic innervation of pancreas beta cells and CLOCK:BMAL1 stimulated insulin secretion. Insulin acts on white adipocytes to stimulate TG uptake—via LPL—and to inhibit lipolysis through inhibition of HSL. Insulin further promotes de novo lipogenesis via activation of chREBPs. Insulin can also reset adipocyte clocks via MAP kinase and PI3 kinase‐dependent upregulation of Per gene expression.
Figure 15. Figure 15. Adipose tissue immune cell‐clock crosstalk in lean and obese conditions. The SCN coordinates adipose physiology through neuronal and endocrine factors affecting, both, adipose tissue immune cell function and adipocyte clocks. (A) In lean subjects, adipose tissue‐resident immunocytes maintain anti‐inflammatory, or type‐2, responses via secretion of immunomodulatory mediators such as IL‐4, IL‐5, IL‐10, IL‐13, and NE. Lean adipocytes mainly release adiponectin and IL‐33 to stabilize this state. (B) In obesity, type‐1 immune responses dominate in adipose tissue immunocytes, leading to chronic adipose tissue inflammation (metaflammation) and insulin resistance. Adipose tissue is infiltrated by proinflammatory immune cells, notably macrophages. At the same time, in response to nutrient overload, adipocytes elevate leptin production, and release proinflammatory cytokines such as TNFα, IL‐1ß, and IL‐6 as well as chemo‐attractants such as CCL2, further recruiting and activating proinflammatory immune cells.


Figure 1. Molecular dynamics of the mammalian clock's core TTL. BMAL1:CLOCK (B and C, respectively) heterodimers bind to E‐Box motifs in the promotor regions of target genes and promote transcription of Period (Per, P) and Cryptochrome (Cry, C) genes in the morning. Over the following hour, PER and CRY proteins accumulate in the cytoplasm and are rapidly degraded following phosphorylation by CK1s and AMPK/GSK3ß, respectively. At the beginning of the dark phase, PER and CRY complexes form, stabilizing both proteins against degradation and initiating translocation into the nucleus. Nuclear PER:CRY complexes inhibit the transactivational activity of BMAL1:CLOCK during the night, thus blocking Per/Cry transcription. Toward the morning, PER and CRY levels in the nucleus decline, releasing BMAL1:CLOCK repression, and initiating a new circadian cycle.


Figure 2. Interlocking TTLs within the mammalian circadian clockwork. The positive limb of the pace making core TTL comprises of the two transcription factors BMAL1 and CLOCK, whereas the PERs and CRYs form its negative limb. Several auxiliary TTLs reinforce stabilization and robustness of the 24‐h oscillation. Rev‐ERBs and RORs repress or stimulate the transcription of Bmal1, respectively. In addition, E4bp4 transcription is regulated by REV‐ERBs/RORs and E4BP4 protein represses Per2 expression. Dbp transcription is activated by BMAL1:CLOCK and DBP activates Per1 transcription via D‐box binding. Transcription of the two Dec genes is regulated by BMAL1:CLOCK and DEC proteins represses CLOCK:BMAL1 transactivation, similar to PER:CRY complexes.


Figure 3. Hierarchical organization of the mammalian circadian clock system. The different clocks within the mammalian organism are organized in a hierarchical manner. A master clock in the SCN receives light information via retinal ipRGC and integrates this information to coordinate circadian rhythms of non‐SCN CNS and peripheral oscillators. The SCN resets peripheral oscillators via regulation of hormonal rhythms (e.g., melatonin), through rhythmic autonomic innervation, or indirectly through the regulation of body temperature and behavioral functions such as sleep/wake and food intake cycles.


Figure 4. Zeitgebers entrain endogenous rhythms to the 24‐h day cycle. (A) The SCN clock controls rest/activity rhythms in rodents. In constant environmental conditions (constant darkness, DD) mice show locomotor free‐running rhythms with periods below 24 h (left). Under 12‐h light: 12‐h dark (LD) cycle locomotor rhythms are entrained to the external 24‐h period (right). (B) Peripheral clock function can be monitored by measuring luminescence from a clock promoter‐driven luciferase construct such as Bmal1:Luc in cultivated cells or tissues. After synchronization tissue clocks free‐run with an endogenous period of close to, but not exactly, 24 h (left). By applying rhythmic temperature cycles these rhythms become entrained to a 24‐h period (right). In a similar way peripheral tissues are entrained by the SCN pacemaker in vivo.


Figure 5. Central and peripheral circadian clocks are synchronized to the 24‐h day by different zeitgebers. Light is the most potent zeitgeber in mammals. Photic information is transmitted to the SCN via ipRGCs. In poikilothermic organisms, temperature fluctuations can also directly affect the circadian pacemaker. Tight coupling of neuronal firing within the SCN resets the SCN clock. From there, time information is passed on to peripheral oscillators. Experiments with transgenic mice have recently shown that SCN clock function is principally not necessary to transmit light information to peripheral clocks, but the mechanisms of this pathway remain largely unclear. In contrast to light, food intake can reset peripheral clocks independent of the SCN via peripheral hormonal and metabolite signals.


Figure 6. Adipose tissue depots. WAT (A, C) and BAT (B, D, E) are differently localized in rodents (A, B) and humans (C‐E). (A) In rodents, WAT is found at subcutaneous, visceral (surrounding the inner organs), and intramuscular sites. Visceral depots are further divided into cervical (in the neck), mesenteric (attached to the intestine), retroperitoneal, perirenal (around the kidney), gonadal, and inguinal (in the groin) pads. (B) BAT is mainly localized between the shoulder blades (interscapular). Smaller depots are found at cervical, axillary, mediastinic, and perirenal sites. (C) In humans, WAT is also principally divided into subcutaneous, visceral, and intramuscular depots. The most prominent subcutaneous WAT depots are localized abdominally and gluteofemorally (at the buttocks and thighs). Visceral depots are spread very broadly throughout the body and divided into pericardial (around the heart), omental (near to the stomach and spleen) peri‐ and pararenal, mesenteric, retroperitoneal, and gonadal pads. (D) In infants large BAT depots are located between the shoulder blades (interscapular), while (E) in adults more widespread, but less distinct depots are found at cervical, interscapular, para‐aortic, paravertebral, and suprarenal sites.


Figure 7. Modern lifestyle factors promote chronodisruption. Different lifestyle factors such as irregular and nighttime food intake, reduced activity, irregular and disrupted sleep and shift work as well as nocturnal exposure to artificial light perturb natural zeitgeber rhythms, disrupting phase coherence between different tissue clocks. Circadian clock misalignment promotes general chronodisruption, promoting the development of various diseases including metabolic dysfunction, cancer, and neuropsychiatric disorders.


Figure 8. Clock gene‐controlled regulation of adipose tissue differentiation. BMAL1:CLOCK regulates BAT adipogenesis through coordination of BMP and TGF‐ß signaling. It also inhibits WAT adipogenesis by activation of WNT pathways. REV‐ERBα induces WAT adipogenesis through stimulation of PPARγ and C/EBPα signaling.


Figure 9. Clock gene‐controlled regulation of WAT lipolysis. Local adipocyte clocks regulate TG breakdown and FFA release through CLOCK:BMAL1 controlled expression of rate limiting enzymes such as HSL, ATGL, and TGH.


Figure 10. Clock gene‐controlled regulation of BAT thermogenesis. BAT circadian oscillators regulate non‐shivering thermogenesis through REV‐ERBα‐mediated suppression of UCP1 expression. At the same time, the BAT clock machinery controls thermogenesis by limiting BAT differentiation through balancing TGF‐ß and BMP signaling in BAT preadipocytes. Of note, the expression of Rev‐erbα itself is downregulated by a thermogenesis inducing cold stimulus.


Figure 11. Adipose specific clock disruption in mice reveals a peripheral feedback mechanism controlling feeding behavior. The SCN synchronizes adipose clocks through endogenous zeitgebers including endocrine factors and behavioral rhythms such as feeding. Adipocyte‐derived and systemic factors together coordinate adipose physiology. Adipocyte‐specific KO of the essential clock gene Bmal1 reveals an adipose clock controlled regulation of polyunsaturated FFA release. Lack of polyunsaturated FFAs in adipose clock‐deficient mice leads to disinhibition of appetite, hyperphagy, and obesity.


Figure 12. The role of GC rhythms in the regulation of WAT physiology. The SCN controls circadian release of GCs from the adrenal via combined neuronal and endocrine pathways. Direct GABAergic projections from the SCN reach the PVN and the subparaventricular zone. From the PVN, CRH is released into the hypophyseal portal system to stimulate secretion of ACTH. ACTH, in turn, induces GC production and secretion in the adrenal cortex. In parallel, from PVN neurons sympathetic ganglia reach via the pituitary and the IML to innervate the adrenal medulla and, to a lesser extent, cortex, regulating sensitivity of the adrenal to ACTH stimulation. Upon binding to GR, GCs exert multiple effects on adipose tissue including the stimulation of lipolysis through activation of ATGL, HSL, and MGLL and of TG uptake through activation of LPL. GCs can also reset adipocyte clocks via induction of Per gene transcription. At the same time, local GC sensitivity is regulated by the adipocyte clock machinery, through CRYs and CLOCK:BMAL1 regulating GR availability and expression, respectively.


Figure 13. The role of melatonin rhythms in the regulation of BAT physiology. SCN regulates circadian rhythms of melatonin release from the pineal gland via a multisynaptic pathway involving the PVN and the IML of the spinal cord. Melatonin can feed back on SCN clock function through MT1/2 signaling. The main regulator of circadian rhythms of BAT activity is the SNS, through activation of ß3‐adrenergic receptor by NE. Melatonin modulates ß3‐AR signaling by inhibiting downstream adenylate cyclase activity and activating CREB through PKC‐mediated signals. At the same time melatonin signaling activates RORa expression through Gaq signaling, which, in turn, counteracts REV‐ERBα‐mediated suppression of UCP1.


Figure 14. The role of insulin in the regulation of WAT physiology. Baseline circadian blood levels of insulin are regulated by the SCN through sympathetic innervation of pancreas beta cells and CLOCK:BMAL1 stimulated insulin secretion. Insulin acts on white adipocytes to stimulate TG uptake—via LPL—and to inhibit lipolysis through inhibition of HSL. Insulin further promotes de novo lipogenesis via activation of chREBPs. Insulin can also reset adipocyte clocks via MAP kinase and PI3 kinase‐dependent upregulation of Per gene expression.


Figure 15. Adipose tissue immune cell‐clock crosstalk in lean and obese conditions. The SCN coordinates adipose physiology through neuronal and endocrine factors affecting, both, adipose tissue immune cell function and adipocyte clocks. (A) In lean subjects, adipose tissue‐resident immunocytes maintain anti‐inflammatory, or type‐2, responses via secretion of immunomodulatory mediators such as IL‐4, IL‐5, IL‐10, IL‐13, and NE. Lean adipocytes mainly release adiponectin and IL‐33 to stabilize this state. (B) In obesity, type‐1 immune responses dominate in adipose tissue immunocytes, leading to chronic adipose tissue inflammation (metaflammation) and insulin resistance. Adipose tissue is infiltrated by proinflammatory immune cells, notably macrophages. At the same time, in response to nutrient overload, adipocytes elevate leptin production, and release proinflammatory cytokines such as TNFα, IL‐1ß, and IL‐6 as well as chemo‐attractants such as CCL2, further recruiting and activating proinflammatory immune cells.
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Article Title: Circadian Rhythms in Adipose Tissue Physiology
 

How to Cite

Jana‐Thabea Kiehn, Anthony H. Tsang, Isabel Heyde, Brinja Leinweber, Isa Kolbe, Alexei Leliavski, Henrik Oster. Circadian Rhythms in Adipose Tissue Physiology. Compr Physiol 2017, 7: 383-427. doi: 10.1002/cphy.c160017